Sex-specific perceptual spaces for a vertebrate basal social aggregative behavior

Loose aggregations of fishes, or shoals, are a basal social organization of vertebrates and offer a valuable opportunity to determine how individual perceptions influence group formation. We used zebrafish, Danio rerio, to comprehensively investigate the preference space for shoaling related to adult pigment pattern variation, presented in the form of 17 zebrafish pigment pattern mutants or closely related species. We examined all combinations of these phenotypes in 2,920 initial and replicated preference tests, and used as subjects both domesticated laboratory stocks and wild-caught fish. By using multidimensional scaling and other approaches, we show that laboratory and wild zebrafish exhibit similar preferences, yet, unexpectedly, these preferences differ markedly between sexes, and also from how human observers perceive the same pigment patterns. Whereas zebrafish males respond to two traits (species and stripe patterning) in deciding whether to join a shoal, zebrafish female preferences do not correlate with a priori identifiable traits, and neither perceptual world is correlated with that of human observers. The observed zebrafish sex differences run counter to the most commonly accepted explanations for the individual selective advantages gained by shoaling. More generally, these data describe very different perceptual worlds between sexes and reveal the importance of sex differences in social group formation, as well as the critical importance of defining species specificity in visual signaling.

[1]  D. Parichy,et al.  Deconstructing evolution of adult phenotypes: genetic analyses of kit reveal homology and evolutionary novelty during adult pigment pattern development of Danio fishes , 2007, Development.

[2]  Stephen L. Johnson,et al.  Mutational analysis of endothelin receptor b1 (rose) during neural crest and pigment pattern development in the zebrafish Danio rerio. , 2000, Developmental biology.

[3]  Stephen L. Johnson,et al.  Zebrafish sparse corresponds to an orthologue of c-kit and is required for the morphogenesis of a subpopulation of melanocytes, but is not essential for hematopoiesis or primordial germ cell development. , 1999, Development.

[4]  Gordon M. Burghardt Foundations of comparative ethology , 1985 .

[5]  Lawrence C. Katz,et al.  Encoding social signals in the mouse main olfactory bulb , 2005, Nature.

[6]  J. Halberstadt The Generality and Ultimate Origins of the Attractiveness of Prototypes , 2006, Personality and social psychology review : an official journal of the Society for Personality and Social Psychology, Inc.

[7]  Jens Krause,et al.  Inter and intra‐population variation in shoaling and boldness in the zebrafish (Danio rerio) , 2003 .

[8]  J. M. Turner,et al.  Pigment pattern evolution by differential deployment of neural crest and post-embryonic melanophore lineages in Danio fishes , 2004, Development.

[9]  E. Shaw The Development of Schooling Behavior in Fishes , 1960, Physiological Zoology.

[10]  Charles M. Breder,et al.  Studies on social groupings in fishes. Bulletin of the AMNH ; v. 117, article 6 , 1959 .

[11]  A. Hurlbert,et al.  Biological components of sex differences in color preference , 2007, Current Biology.

[12]  R. R. Krausz Living in Groups , 2013 .

[13]  Michael J. Ryan,et al.  Timing and plasticity of shoaling behaviour in the zebrafish, Danio rerio , 2007, Animal Behaviour.

[14]  Patrick J. F. Groenen,et al.  Modern Multidimensional Scaling: Theory and Applications , 2003 .

[15]  G. Gerlach,et al.  The behaviour and ecology of the zebrafish, Danio rerio , 2007, Biological reviews of the Cambridge Philosophical Society.

[16]  R. Wassersug,et al.  Tadpole behaviour: aggregation in larval Xenopus laevis. , 1971, Animal behaviour.

[17]  John D. Storey,et al.  Statistical significance for genomewide studies , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[18]  K. I. Gabriel,et al.  Sex differences in cue perception in a visual scene: investigation of cue type. , 2007, Behavioral neuroscience.

[19]  R. Greil,et al.  Multidimensional scaling as a tool for analysing quality of life data , 2002, Quality of Life Research.

[20]  E. Martins,et al.  The effects of early and adult social environment on zebrafish (Danio rerio) behavior , 2007, Environmental Biology of Fishes.

[21]  Stephen L. Johnson,et al.  nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. , 1999, Development.

[22]  T. Pitcher Behaviour of Teleost Fishes , 1986 .

[23]  M. Ryan,et al.  Learned Social Preference in Zebrafish , 2004, Current Biology.

[24]  J. Krause,et al.  QTL Analysis of Behavioral and Morphological Differentiation Between Wild and Laboratory Zebrafish (Danio rerio) , 2006, Behavior genetics.

[25]  D. Parichy Evolution of danio pigment pattern development , 2006, Heredity.

[26]  Ian K Quigley,et al.  Evolutionary diversification of pigment pattern in Danio fishes: differential fms dependence and stripe loss in D. albolineatus , 2004, Development.

[27]  M. Ryan,et al.  Directional Patterns of Female Mate Choice and the Role of Sensory Biases , 1992, The American Naturalist.

[28]  S. Hamann,et al.  Men and women differ in amygdala response to visual sexual stimuli , 2004, Nature Neuroscience.

[29]  C. Carlson,et al.  Effect of cross-rearing on species identification in zebra fish and pearl danios. , 1982, Developmental psychobiology.

[30]  W. Rowland,et al.  A potential model system for studying the genetics of domestication: behavioral variation among wild and domesticated strains of zebra danio (Danio rerio) , 2005 .

[31]  L. Edelstein-Keshet,et al.  Complexity, pattern, and evolutionary trade-offs in animal aggregation. , 1999, Science.

[32]  H. A. David,et al.  The method of paired comparisons , 1966 .

[33]  Myron Wish,et al.  Three-Way Multidimensional Scaling , 1978 .

[34]  M. Ryan,et al.  SEXUAL SELECTION IN FEMALE PERCEPTUAL SPACE: HOW FEMALE TUNGARA FROGS PERCEIVE AND RESPOND TO COMPLEX POPULATION VARIATION IN ACOUSTIC MATING SIGNALS , 2003, Evolution; international journal of organic evolution.

[35]  D. Parichy,et al.  Zebrafish in the wild: a review of natural history and new notes from the field. , 2007, Zebrafish.

[36]  P. Groenen,et al.  Modern multidimensional scaling , 1996 .

[37]  Stephen L. Johnson,et al.  An orthologue of the kit-related gene fms is required for development of neural crest-derived xanthophores and a subpopulation of adult melanocytes in the zebrafish, Danio rerio. , 2000, Development.

[38]  P. Hudson,et al.  Paddlefish (Polyodon spathula): Growth and Food of Young of the Year and a Suggested Technique for Measuring Length , 1977 .